Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Bioaugmentation-assisted phytoremediation of manganese and cadmium co-contaminated soil by Polygonaceae plants (Polygonum hydropiper L. and Polygonum lapathifolium L.) and Enterobacter sp. FM-1



Polygonum hydropiper L. and Polygonum lapathifolium L. are two of the well-known indigenous Mn-hyperaccumulators. Enterobacter sp. FM-1 is a plant growth-promoting bacterium (PGPB) that we found in our previous study. We intended to develop a novel strategy to improve Mn and Cd co-contaminated soil phytoremediation by using a Mn and Cd-resistant bacterium for soil bioaugmentation.


We carried out this study to investigate the effects of different Enterobacter sp. FM-1 inoculation concentrations (0, 5.0 × 105, 1.0 × 106 and 1.4 × 106 CFU g−1 soil) on the phytoremediation of Mn and Cd by Polygonum hydropiper L. and Polygonum lapathifolium L. in two types of Mn-Cd co-contaminated soil.


In both soils, inoculation with Enterobacter sp. FM-1 promoted the growth of both plants. Moreover, inoculation with Enterobacter sp. FM-1 (≥1.0 × 106 CFU g−1 soil) significantly increased soil Mn and Cd bioavailability and decreased the soil pH. Therefore, inoculation with Enterobacter sp. FM-1 (1.4 × 106 CFU g−1 soil) improved Mn and Cd accumulation in both plants. Polygonum hydropiper L. presented excellent Mn accumulation in both soils. Additionally, both plants exhibited strong translocation and excellent phytoextraction and bioaccumulation abilities for Mn and Cd.


Our findings indicated that Enterobacter sp. FM-1 is a potent bioaugmentation agent that facilitates Mn and Cd phytoextraction in Polygonum hydropiper L. and Polygonum lapathifolium L.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3


  1. Abou-Shanab RA et al (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224

  2. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals--concepts and applications. Chemosphere 91:869–881

  3. Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

  4. Baker AJM, Brooks RR (1989) Terrestrial higher plants which hyperaccumulate metallic elements-a review of their distribution, ecology and phytochemistry. Biorecovery 1:81–126

  5. Becerracastro C, Monterroso C, Prietofernández A, Rodríguezlamas L, Loureiroviñas M, Acea MJ, Kidd PS (2012) Pseudometallophytes colonising Pb/Zn mine tailings: a description of the plant-microorganism-rhizosphere soil system and isolation of metal-tolerant bacteria. J Hazard Mater 217-218:350–359

  6. Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250

  7. Bidwell SD, Woodrow IE, Batianoff GN, Sommerknudsen J (2002) Hyperaccumulation of manganese in the rainforest tree Austromyrtus bidwillii (Myrtaceae) from Queensland, Australia. Funct Plant Biol 29:899–905

  8. Bolan N, Kunhikrishnan A, Thangarajan R, Kumpiene J, Park J, Makino T, Kirkham MB, Scheckel K (2014) Remediation of heavy metal(loid)s contaminated soils--to mobilize or to immobilize? J Hazard Mater 266:141–166

  9. Carter MR (1993) Soil sampling and methods of analysis. J Environ Qual 38:15–24

  10. Chen L, Luo S, Li X, Wan Y, Chen J, Liu C (2014) Interaction of cd-hyperaccumulator Solanum nigrum L. and functional endophyte Pseudomonas sp. Lk9 on soil heavy metals uptake. Soil Biol Biochem 68:300–308

  11. Elshamy MM, Heikal YM, Bonanomi G (2019) Phytoremediation efficiency of Portulaca oleracea L. naturally growing in some industrial sites, Dakahlia District, Egypt. Chemosphere 225:678–687

  12. Faust MB, Christians NE (2000) Copper reduces shoot growth and root development of creeping bentgrass. Crop Sci 40:498–502

  13. Fernando DR, Guymer G, Reeves RD, Woodrow IE, Baker AJ, Batianoff GN (2009) Foliar Mn accumulation in eastern Australian herbarium specimens: prospecting for 'new' Mn hyperaccumulators and potential applications in taxonomy. Ann Bot-london 103:931–939

  14. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

  15. Grigatti M, Dios PM, Blok WJ, Ciavatta C, Veeken A (2007) A standardized method for the determination of the intrinsic carbon and nitrogen mineralization capacity of natural organic matter sources. Soil Biol Biochem 39:1493–1503

  16. Guo J, Chi J (2014) Effect of cd-tolerant plant growth-promoting rhizobium on plant growth and cd uptake by Lolium multiflorum lam. And Glycine max (L.) Merr. In cd-contaminated soil. Plant Soil 375:205–214

  17. Guo J, Feng R, Ding Y, Wang R (2014) Applying carbon dioxide, plant growth-promoting rhizobacterium and EDTA can enhance the phytoremediation efficiency of ryegrass in a soil polluted with zinc, arsenic, cadmium and lead. J Environ Manag 141:1–8

  18. He H, Ye Z, Yang D, Yan J, Xiao L, Zhong T, Yuan M, Cai X, Fang Z, Jing Y (2013) Characterization of endophytic Rahnella sp. JN6 from Polygonum pubescens and its potential in promoting growth and cd, Pb, Zn uptake by Brassica napus. Chemosphere 90:1960–1965

  19. Jing YX et al (2014) Characterization of Bacteria in the Rhizosphere soils of Polygonum Pubescens and their potential in promoting growth and cd, Pb, Zn uptake by Brassica napus. International Journal of Phytoremediation 16:321–333

  20. Khaokaew S, Landrot G (2015a) A field-scale study of cadmium phytoremediation in a contaminated agricultural soil at Mae Sot District, Tak Province, Thailand: (1) determination of cd-hyperaccumulating plants. Chemosphere 138:883–887

  21. Khaokaew S, Landrot G (2015b) A field-scale study of cadmium phytoremediation in a contaminated agricultural soil at Mae Sot District, Tak Province, Thailand: (1) determination of cd-hyperaccumulating plants. Chemosphere 138:883

  22. Lai YP, Li MS, Yang SX, Chen CQ, Li Y (2006) Heavy metal concentrations in soils and main agronomic crops in restored Bayi manganese mine, Guangx i. Mineral Resource and Geology 20:651–655

  23. Li X, Zhang X, Wang X, Yang X, Cui Z (2019) Bioaugmentation-assisted phytoremediation of lead and salinity co-contaminated soil by Suaeda salsa and Trichoderma asperellum. Chemosphere 224:716–725

  24. Li Y, Liu KH, Wang Y, Zhou ZM, Chen CS, Ye PH, Yu FM (2018) Improvement of cadmium phytoremediation by Centella asiatica L. after soil inoculation with cadmium-resistant Enterobacter sp. FM-1. Chemosphere 202:280–288

  25. Liu J, Shang W, Zhang X, Zhu Y, Ke Y (2014a) Mn accumulation and tolerance in Celosia argentea Linn.: a new Mn-hyperaccumulating plant species. J Hazard Mater 267:136–141

  26. Liu J, Zhang X, Li T, Wu Q, Jin Z (2014b) Soil characteristics and heavy metal accumulation by native plants in a Mn mining area of Guangxi, South China. Environ Monit Assess 186:2269–2279

  27. Liu KH, Yu FM, Chen ML, Zhou ZM, Chen CS, Li MS, Zhu J (2016) A newly found manganese hyperaccumulator—Polygonum lapathifolium Linn. Int J Phytoremediat 18:348–353

  28. Losfeld G, L’Huillier L, Fogliani B, Coy SM, Grison C, Jaffré T (2015) Leaf-age and soil-plant relationships: key factors for reporting trace-elements hyperaccumulation by plants and design applications. Environ Sci Pollut R 22:5620–5632

  29. Ma Y, Oliveira RS, Nai F, Rajkumar M, Luo Y, Rocha I, Freitas H (2015) The hyperaccumulator Sedum plumbizincicola harbors metal-resistant endophytic bacteria that improve its phytoextraction capacity in multi-metal contaminated soil. J Environ Manag 156:62–69

  30. Nie L, Shah S, Rashid A, Burd GI, George Dixon D, Glick BR (2002) Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiol Biochem 40:355–361

  31. Prapagdee B, Chanprasert M, Mongkolsuk S (2013) Bioaugmentation with cadmium-resistant plant growth-promoting rhizobacteria to assist cadmium phytoextraction by Helianthus annuus. Chemosphere 92:659

  32. Rajkumar M, Freitas H (2008) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71:834–842

  33. Rojjanateeranaj P, Sangthong C, Prapagdee B (2017) Enhanced cadmium phytoremediation of Glycine max L. through bioaugmentation of cadmium-resistant bacteria assisted by biostimulation. Chemosphere 185:764–771

  34. Sangthong C, Setkit K, Prapagdee B (2016) Improvement of cadmium phytoremediation after soil inoculation with a cadmium-resistant Micrococcus sp. Environ Sci Pollut Res 23:756–764

  35. Sheng X-F, Xia J-J, Jiang C-Y, He L-Y, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170

  36. Singh J, Kalamdhad AS (2013) Bioavailability and leachability of heavy metals during water hyacinth composting. Chem Speciat Bioavaila 25:1–14

  37. Sun WH, Xiong Z, Chu L, Li W, Soares MA, White JF Jr, Li HY (2019) Bacterial communities of three plant species from Pb-Zn contaminated sites and plant-growth promotional benefits of endophytic Microbacterium sp. (strain BXGe71). J Hazard Mater 370:225–231

  38. Ullah A, Sun H, Munis MFH, Fahad S, Yang X (2015) Phytoremediation of heavy metals assisted by plant growth promoting (PGP) bacteria: a review. Environ Exp Bot 117:28–40

  39. Walkley AJ, Black IA (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci 37:29–38

  40. Wang H, Tang S, Liao X, Cao Q, Yang A (2007) A new manganese-hyperaccumulator: Polygonum hydropiper L. Ecol Environ 16:830–834

  41. Wei Y et al (2014) Molecular diversity of arbuscular mycorrhizal fungi associated with an Mn hyperaccumulator -- Phytolacca americana , in Mn mining area. Appl Soil Ecol 82:11–17

  42. Xue S, Wang J, Wu C, Li S, Hartley W, Wu H, Zhu F, Cui M (2018) Physiological response of Polygonum perfoliatum L. following exposure to elevated manganese concentrations. Environ Sci Pollut Res 25:132–140

  43. Xue SG, Chen YX, Reeves RD, Baker AJ, Lin Q, Fernando DR (2004) Manganese uptake and accumulation by the hyperaccumulator plant Phytolacca acinosa Roxb. (Phytolaccaceae). Environ Pollut 131:393–399

  44. Yang QW, Ke HM, Liu SJ, Zeng Q (2018) Phytoremediation of Mn-contaminated paddy soil by two hyperaccumulators (Phytolacca americana and Polygonum hydropiper) aided with citric acid. Environ Sci Pollut Res 25:25933–25941

  45. Yang QW, Zeng Q, Xiao F, Liu XL, Pan J, He JF, Li ZY (2013) Investigation of manganese tolerance and accumulation of two Mn hyperaccumulators Phytolacca americana L. and Polygonum hydropiper L. in the real Mn-contaminated soils near a manganese mine. Environ Earth Sci 68:1127–1134

  46. Yang SX, Deng H, Li MS (2008) Manganese uptake and accumulation in a Woody Hyperaccumulator, Schima Superba. Plant Soil Environ 54:441–446

  47. Yang SX, Li MS, Li Y, Huang HR (2006) Study on heavy metal pollution in soil and plants and ecological recovery in Guangxi Pingle manganese mine. Mining Saf Environ Protect 33:21–23

  48. Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464

  49. Yu F, Liu K, Ye P, Zhou Z, Li Y (2019) Manganese tolerance and accumulation characteristics of a woody accumulator Camellia oleifera. Environ Sci Pollut Res 26:21329–21339

  50. Yu FM, Yu QP, Liu KH, Wang Y, Zhou ZM, Chen CS, Li Y (2018) Improvement of cadmium-contaminated soil phytoremediation by Centella asiatica L. through bioaugmentation of Enterobacter sp. FM-1. China Environ Sci 38:4625–4630

  51. Zhang WH, Chen W, He LY, Wang Q, Sheng XF (2015) Characterization of Mn-resistant endophytic bacteria from Mn-hyperaccumulator Phytolacca americana and their impact on Mn accumulation of hybrid penisetum. Ecotoxicol Environ Saf 120:369–376

Download references


This paper is sponsored by the National Key Research and Development Project (grant number 2017YFD0801500), the National Natural Science Foundation of China (grant numbers 41967019, 41907096, and 41661077) and the Natural Science Foundation of Guangxi (grant number 2018JJA150018).

Author information

Correspondence to Kehui Liu or Fangming Yu.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Juan Barcelo.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Lin, J., Huang, Y. et al. Bioaugmentation-assisted phytoremediation of manganese and cadmium co-contaminated soil by Polygonaceae plants (Polygonum hydropiper L. and Polygonum lapathifolium L.) and Enterobacter sp. FM-1. Plant Soil (2020).

Download citation


  • Enterobacter sp. FM-1
  • Manganese
  • Cadmium
  • Polygonum hydropiper L
  • Polygonum lapathifolium L